Case Control Study
Copyright ©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Oncol. Nov 15, 2019; 11(11): 998-1010
Published online Nov 15, 2019. doi: 10.4251/wjgo.v11.i11.998
Toll-like receptor 9 polymorphisms and Helicobacter pylori influence gene expression and risk of gastric carcinogenesis in the Brazilian population.
Manoela Dias Susi, de Matos Lourenço Caroline, Lucas Trevizani Rasmussen, Spencer Luis Marques Payão, Ana Flávia Teixeira Rossi, Ana Elizabete Silva, Juliana Garcia de Oliveira-Cucolo
Manoela Dias Susi, de Matos Lourenço Caroline, Department of Graduate-Level Research, USC-Sacred Heart University, Bauru 17011-970, SP, Brazil
Lucas Trevizani Rasmussen, Spencer Luis Marques Payão, Department of Genetics and Molecular Biology, FAMEMA-Marilia Medical School, Marília 17519-030, SP, Brazil
Ana Flávia Teixeira Rossi, Ana Elizabete Silva, Department of Biology, São Paulo State University-UNESP, São José do Rio Preto 15054-000, SP, Brazil
Juliana Garcia de Oliveira-Cucolo, Department of Molecular, Biological and Genetics and Molecular Biology Research Unit – UPGEM, Faculty of Medicine of São José do Rio Preto – FAMERP, São José do Rio Preto 15090-000, SP, Brazil.
Author contributions: Oliveira-Cucolo JG and Silva AE conceived and designed the experiments; Susi MD, de Matos Lourenço C, Rossi AFT and Oliveira-Cucolo JG performed the experiments; Oliveira-Cucolo JG, Silva AE and Rossi AFT analyzed and interpreted the data; Rasmussen LT, Payão SLM and Silva AE contributed with the collection of samples/reagents/materials and analysis tools; Oliveira-Cucolo JG, Rossi AFT and Silva AE drafted the manuscript and revised it; All of the authors have approved the final version of manuscript for publication.
Supported by The São Paulo Research Foundation (FAPESP), NO. 2013/14022-6 and NO. 2014/17716-1.
Institutional review board statement: This study was approved by the research ethics committee of USC-Sacred Heart University.
Informed consent statement: Informed consent was obtained from each patient.
Conflict-of-interest statement: The authors declare that they have no conflict of interest.
Data sharing statement: Participants gave written informed consent for data sharing.
STROBE statement: The manuscript was prepared and revised according to the STROBE Statement-checklist of items.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Ana Elizabete Silva, PhD, Adjunct Professor, Department of Biology, São Paulo State University-UNESP, Rua Cristóvão Colombo 2265, São José do Rio Preto 15054-000, SP, Brazil. ae.silva@unesp.br
Telephone: +55-17-32212384 Fax: +55-17-322212390
Received: March 14, 2019
Peer-review started: March 14, 2019
First decision: May 9, 2019
Revised: July 26, 2019
Accepted: August 27, 2019
Article in press: August 27, 2019
Published online: November 15, 2019
Processing time: 246 Days and 13.2 Hours
ARTICLE HIGHLIGHTS
Research background

Gastric cancer (GC) is one of the most prevalent cancers worldwide, with high rates of incidence and death. It ranks sixth in the world and is the fifth leading cause of cancer-related deaths worldwide. In Brazil, GC is the fourth most frequent type of cancer in men, and the sixth in women, with an estimated incidence of 21,290 new cases in 2018. The main risk factor associated with this type of cancer is the infection by the bacterium Helicobacter pylori (H. pylori). Toll-like receptors are the first line of host defense, and are involved in H. pylori recognition and activation of the inflammatory and carcinogenic process. The presence of single nucleotide polymorphisms (SNPs) in genes that activate the immune response may modulate the risk of precancerous lesions and GC, among them of which is TLR9 polymorphisms.

Research motivation

Polymorphisms in toll-like receptors genes have emerged with a risk factor of infectious diseases and cancer. However, the literature presents conflicting results. Therefore, several studies are needed to assess and confirm the real role among factors that influence changes in immune inflammatory processes related to GC, especially when it is a mixed population such as the Brazilian population.

Research objectives

Considering the inconsistent results and the importance of these receptors in the immune response and to susceptibility to inflammatory diseases and cancer, new studies are needed. Thus, the aim of this study was to evaluate whether the TLR9-1237 TC (rs5743836) and TLR9-1486 CT (rs187084) polymorphisms (alone and in combination) are associated with a risk of chronic gastritis (CG) and GC. In addition, we also evaluate the influence of both polymorphisms and H. pylori infection on TLR9 mRNA expression. The results may highlight important polymorphisms that act on gastric carcinogenesis.

Research methods

A case-control study was conducted to evaluate two TLR9 SNPs (TLR9-1237 TC-rs5743836 and TLR9-1486 CT-rs187084) in CG and GC patients. A total of 609 DNA samples of peripheral blood [248 CG, 161 GC, and 200 samples from healthy individuals (C)] were genotyped by polymerase chain reaction-restriction fragment length polymorphism. All samples were tested for the H. pylori infection using Hpx1 and Hpx2 primers. Quantitative polymerase chain reaction by TaqMan® assay was used to quantify TLR9 mRNA from fresh gastric tissues (48 GC, 26 CG, and 14 C).

Research results

The data showed that for TLR9-1237, the TC + CC or CC genotypes were associated with a higher risk of GC than the C and CG groups. For TLR9-1486, an association between the CT + TT genotypes and increased risk of both GC and CG was observed when compared to the C group. Moreover, the presence of TLR9-1237 TC/CC + TLR9-1486 CC genotypes potentiates the risk for this neoplasm. The TLR9 mRNA level was significantly higher in the GC group in relation to the CG group and normal mucosa. When the samples were grouped according to the polymorphic genotypes and the presence of H. pylori infection, an influence of TLR9-1237 TC + CC polymorphic genotypes and H. pylori infection was observed on the upregulation of mRNA expression.

Research conclusions

Our findings highlight that the functional polymorphisms of the TLR9-1237 T/C (rs5743836) and TLR9-1486 C/T (rs187084) receptors are associated with an increased risk of developing premalignant and malignant gastric diseases in this Brazilian population, and therefore may act as a potential factor in the progression of gastric carcinogenesis. TLR9 mRNA expression levels are upregulated in GC tissues and are modulated by both H. pylori infection and the presence of TLR9-1237 TC + CC-variant genotypes. The pattern of the host’s immune response, along with genetic and environmental factors, are essential for understanding the pathology of GC. Thus, polymorphisms in genes that affect its expression, such as TLR9, could have an effect on the development and clinical manifestation of disease.

Research perspectives

Considering that most cases of GC have a good prognosis and are treatable when diagnosed at an early stage, it is of the utmost importance to establish molecular markers capable of identifying risk groups and providing early diagnosis in individuals with increased risk of developing this neoplasm. Overall, our results indicate that the TLR9 gene plays an important role in gastric carcinogenesis, highlighting the importance of the TLR9-1237 T/C (rs5743836) polymorphism in increasing gene expression and H. pylori infection, possibly triggering a stronger inflammatory response, which in turn enhances the risk of tumor progression. In the future, it would be important to investigate another polymorphism in the TLR9 gene [TLR9-2848 C/T (rs352140)], described in the literature as associated with cancer, but not yet analyzed in our Brazilian population.